BOLETINDE LA ASOCIACION HERPETOLOGICA ESPAÑOLAn.º 17 (1) - julio 2006

Bol. Asoc. Herpetol. Esp. (2006) 17 (1)

54

GASTROINTESTINAL PARASITES IN SAURIANS FROMSOME CENTRAL MEDITERRANEAN ISLANDS

VICENTE ROCA,1 PIETRO LO CASCIO 2 & JUAN MARTIN 1

1 Departament de Zoología. Facultat de Ciències Biològiques. Universitat de València.Dr. Moliner, 50. 46100 Burjassot. València. Spain.

2 Associacione Nesos. Via Vittorio Emanuele, 24. 98055 Lipari (ME). Italy.e-mail: vicente.roca@uv.es

Key words: Parasites, saurians, Mediterranean islands.

Resumen: Se ha llevado a cabo un estudio helmintológico de muestras fecales de tresespecies de saurios (Podarcis filfolensis, Podarcis raffonei y Chalcides ocellatus) en islas delNorte y Sur de Sicilia (Mediterráneo Central). Se detectaron cuatro especies de nematodos,Parapharyngodon micipsae, Parapharyngodon sp., Pharyngodon sp. y Skrjabinelazia sp. Losresultados obtenidos sugieren, para los tres hospedadores, pobreza de sus comunidadeshelmintianas y hábitos alimenticios esencialmente carnívoros.

The islands of Central Mediterraneanharbour several lizard species, includingseveral ones which are endemic of macro- andmicro-insular systems. Parasitological studieson these populations could result of specialinterest due to the peculiar zoogeographicaland ecological characteristics related to thehosts, such as isolation, high populationdensities, and feeding habits (Pérez-Mellado &Corti, 1993; Brown & Pérez-Mellado, 1994;Van Damme,1999; Carretero, 2004).

However, the parasites of these popula-tions have not been so far investigated and,in general, data on Mediterranean lizards arestill scarce and referred mainly to thelacertids of the genus Podarcis (Hornero,1991; Roca, 1993, 1995, 2004).

In this paper the results of someinvestigations concerning two species ofLacertidae, Podarcis filfolensis (Bedriaga,1876) and Podarcis raffonei (Mertens, 1952),and one of Scincidae, Chalcides ocellatus(Forskal, 1775), are discussed.

MATERIALS AND METHODS

Study areaThe present research concerns the

parasites of lizard populations occurring onthree circum-Sicilian islets: Lampione, thesmallest of the Pelagie Islands group(Channel of Sicily); Scoglio Faraglione andStrombolicchio, two tiny islets belonging tothe Aeolian Archipelago (S Tyrrhenian)(Figure 1).

Lampione (35°33’00”N / 12°19’11”EGreenwich, 17 Km off the W coast ofLampedusa Island) has a surface of 21 000m2 and a maximum elevation of 36 m. Thevegetation is dominated by halo-nitrophilousperennial shrubs (Arthrocnemummacrostachyum) and high temporal herbs(Lavatera arborea), due to the occurrence ofa large colony of Mediterranean Yellow-legged Gull, Larus cachinnans, whichinduces a strong level of eutrophication andnutrient imbalances on the soil.

PARASITOLOGÍA

Bol. Asoc. Herpetol. Esp. (2006) 17 (1)

55

Scoglio Faraglione (38°34’77”N /14°48’08”E, 300 m off the W coast of SalinaIsland) has a surface of 4900 m2 and amaximum elevation of 35 m. The top of theislet is covered by a dense epi-littoralvegetation, referred to the Senecioni-Helichrysetum litorei.

Strombolicchio (38°49’07”N / 15°15’13”E,1.5 Km off the NE coast of Stromboli Island)has a surface of 3000 m2 and a maximumelevation of 49 m. Its perimeter is formed byvery steep cliffs, sparsely covered bychasmophylous formations referred toHyoseridetum taurinae-dianthetosum aeolici,while on the top spots of maquis ofEuphorbia dendroides also occur.

The studied islets are nowadaysuninhabited, even if Lampione and Strom-bolicchio have been partially anthropisedduring the building of lighthouses.

Studied speciesThe saurian hosts parasitologically

investigated are Chalcides ocellatus,Podarcis filfolensis and Podarcis raffonei.

C. ocellatus, is widespread throughout NAfrica, some areas of Asia (from Middle Eastto western Pakistan) and S Europe, where it

occurs on several islands (such as Crete,Rhodes, Maltese Archipelago, Sicily,Sardinia and their satellites: Schneider,1997). It is one of the most common lizardsin the Pelagie Islands, and the Lampionepopulation is characterised by high densityand an unusual rather high proportion ofvegetal matter included in the diet (P. LoCascio, unpublished data).

P. filfolensis is endemic of the MalteseArchipelago and also occurs on somePelagie Islands (Linosa, Lampione, andrecently discovered on Lampedusa, LoCascio et al., 2005), where it was probablyintroduced (Bischof, 1997). Lampione Isletrepresents the westernmost site of thedistributional range of the species, where itshows a very high population density. Partialherbivorism is well known for this species (LoCascio et al., 2004; Bombi et al., 2005).

P. raffonei is endemic of the AeolianArchipelago and is considered one of themost threatened species of theMediterranean fauna, due to its restricteddistribution, limited to three tiny islets(Strombolicchio, Scoglio Faraglione and LaCanna) and to few small areas of VulcanoIsland (Capula & Lo Cascio, 2006). The

Figure 1. Localization of the searched lizard populations.

Bol. Asoc. Herpetol. Esp. (2006) 17 (1)

56

islets’ populations are characterised by lowdensity. This species is known as a strictlyinsectivorous lizard (Luiselli et al., 2004),even if further investigations suggested theoccurrence of a partial herbivorism in somemicro-insular environments (P. Lo Cascio,unpublished data).

MethodsThe lizards were noosed or captured by

hand, then measured and sexed. Faecalremains were obtained during theirexamination. No specimens were sacrifiedduring the present study. The faecal pelletsand the parasites were preserved in alcoholand successively examined in laboratoryunder a stereoscope. Parasites wereexamined under optical microscope.

RESULTS AND DISCUSSION

Four nematode species were found in allof three host species examined. Three ofthem, Parapharyngodon micipsae (Seurat,1917), Pharyngodon sp. andParapharyngodon sp., belong to the familyPharyngodonidae, and the other,Skrjabinelazia sp. belongs to Seuratidae(Chabaud, 1974; Petter & Quentin, 1976).

Number of individuals, sex of the hosts andlocalities in which nematodes were found,are indicated in Table 1.

Nematodes belonging to these genus andspecies are usually found in skinks fromNorth Africa (Ashour et al., 1992; Al Deen etal., 1995; Ibrahim et al., 2005) and in severalspecies of Podarcis, lizards from Europe(Roca, 1985; Hornero, 1991; Roca, 1995;Martin, 2005). Nevertheless, as P. raffoneihas been helminthologically searched for thefirst time, it is a new host for P. micipsae,Parapharyngodon sp. and Skrjabinelazia sp.

Roca (1995) found homogeneus helminthfauna in Mediterranean insular lizards, inaccordance with the hypothesis of Alcover(1988) regarding the common origin of theselizards. Roca (loc. cit.) suggested lowdiversity for the helminth communities ofthese insular hosts, in agreement with thetypical pattern of helminth infection of manyreptiles (Roca & Hornero, 1994), althoughslight differences may be found amongseveral islands and hosts (Roca & Hornero,1994; Roca, 1995).

This preliminary study does not includedata of prevalence or intensity of helminthsbecause the methodology used forhelminthological analysis is an indirectmethod. But, taking into account the number

Table 1. Intestinal parasites found in sampled hosts.

ReferenceHost Sex Locality Date

Parasitecode found

1 P. raffonei M Scoglio, Faraglione 02/05/05 P. micipsae (1 ; 2 )2 “ H Strombolicchio 29/03/05 Parapharyngodon sp (3 ) 3 “ H “ 04/10/05 Parapharyngodon sp (1 ) 4 “ M “ 04/10/04 Parapharyngodon sp (4 ) 5 “ H “ 04/10/04 Skrjabinelazia sp (1 ) 6 “ M “ 04/10/04 Skrjabinelazia sp (2 ) 7 “ M “ 08/09/04 Parapharyngodon sp (4 ) – “ M “ 21/06/05 Parapharyngodon sp (1 ) 2 P. filfolensis M Lampione 16/09/05 Pharyngodon sp (1 ) 1 C. ocellatus – “ 02/06/04 Pharyngodon sp (1 ; 1 ) 3 “ – “ 16/09/05 Parapharyngodon sp (1 ) 4 “ – “ 16/09/05 Parapharyngodon sp (1 ) 5 “ – “ 21/05/05 Skrjabinelazia sp (7 )

Bol. Asoc. Herpetol. Esp. (2006) 17 (1)

57

of species and individuals found, we can alsopredict poor helminth communities in the treeexamined hosts in agreement with the resultsof Roca (1995) for other Mediterraneanspecies and islands. This typical pattern ofpoor helminth communities is related withseveral features of these reptile hosts, asectothermy, simplicity of the alimentarycanal, low vagility and simple diet (Kennedyet al., 1986; Roca & Hornero, 1994).

Pharyngodonid nematodes found insearched hosts are typical of the carnivorousreptiles (Petter & Quentin, 1976; Martin et al.,2005). Thus, although tendency to herbivoryis reported for P. filfolensis, and has beenreported in other insular lacertids, e.g.Podarcis lilfordi and Podarcis pityusensisfrom the Balearic Islands (Pérez-Mellado &Corti, 1993; Roca & Hornero, 1994), ourresults suggest that P. filfolensis, P. raffoneiand C. ocellatus are primarily carnivorousbeing the tendency to herbivorism asecondary adaptation (Roca, 1996) related tothe trophic availability and to the evolutionaryage of the lizard populations on each island.

REFERENCES

Alcover, J.A. 1988. Las faunas paleolíticas de las islasmediterráneas. Mundo Científico, 80: 504-517.

Al Deen, A., Al Shareef, M.F. & Saber, S.A. 1995.Ecological studies of Chalcides ocellatus (Forskal,1775) and Hemidactylus turcicus (Linnaeus, 1758)from Egypt with special reference to helminthparasites. Journal of Egyptian Society ofParasitology, 25: 145-156.

Ashour, A.A., Koura, E.A., El-Alfy, N.M. & Abdel Aal, Z.1992. On the morphology of the Oxyurid nematodePharyngodon mamillatus (Linstow, 1897) fromChalcides ocellatus from Egypt. Journal of theEgyptian Society of Parasitology, 22: 801-807.

Bischoff, W. 1997. Podarcis filfolensis (Bedriaga, 1876).276-277. In: Gasc, J.P. (ed.), Atlas of Amphibiansand Reptiles in Europe. SEH - Múseum Nationald’Histoire Naturelle. Paris.

Bombi, P., Vignoli, L., Scalera, R. & Bologna, M.A. 2005.Food habits of Podarcis filfolensis (Reptilia,Lacertidae) on a small Mediterranean island duringthe dry season. Amphibia-Reptilia, 26: 412-417.

Brown, R.P. & Pérez-Mellado, V. 1994. Ecologicalenergetics and food acquisition in dense Menorcanislet populations of the lizard Podarcis lilfordi.Functional Ecology, 8: 427-434.

Capula, M. & Lo Cascio, P. 2006. Podarcis raffonei(Mertens, 1952). 480-485. In: Sindaco, R., Doria, G.,Razzetti, E. & Bernini, F. (eds.), Atlante degli Anfibie dei Rettili d’Italia. Polistampa. Firenze.

Carretero, M.A. 2004. From set menu to a la carte.Linking issues in trophic ecology of Mediterraneanlacertids. Italian Journal of Zoology. Supplement, 2:121-133.

Chabaud, A.G. 1974. Class Nematoda. Key tosubclasses, orders and superfamilies. 1-17. In:Anderson, R.C., Chabaud, A.G. & Willmot, S. (eds.),C.I.H. Keys to the Nematode Parasites ofVertebrates. Commonwealth Agricultural Bureaux,Farnham Royal. Bucks. England.

Hornero, M.J. 1991. Helmintofauna de los Lacértidosendémicos de las Islas Baleares (MediterráneoOccidental). Ph. D. Thesis University of Valencia.

Ibrahim, H.M.S., Fadiel, M.M. & Nair, G.A. 2005.Gastrointestinal helminths of the lizard Chalcidesocellatus from Benghazi, Lybia. Journal ofHelminthology, 79: 35-39.

Kennedy, C.R., Bush, A.O. & Aho, J.M. 1986. Patterns inhelminth communities: why are birds and fishdifferent? Parasitology, 93: 205-215.

Lo Cascio, P., Luiselli, L. & Corti, C. 2004. Preliminarydata on the ecology of Podarcis filfolensis atLampione Islet (Pelagie Islands, Channel of Sicily).25. In: Corti, C. & Lo Cascio P. (eds.), Abstracts ofthe 5th International Symposium on the Lacertids ofthe Mediterranean Basin. Lipari, Italy, 7-11 May2004. Florence University Press. Firenze.

Lo Cascio, P., Corti, C., Billeci, V. & Nicolini, G. 2005.“First came, first served”, or the recent introducedlizard populations of Lampedusa Island (S Italy).Abstracts of the 13th Ordinary General Meeting ofthe Societas Europaea Herpetologica. Bonn,Germany, 27 September-2 October 2005.

Luiselli, L., Capula, M., Corti, C., Lo Cascio, P. & Pérez-Mellado, V. 2004. Preliminary data on the feedingecology of Podarcis raffonei (Reptilia, Lacertidae), athreatened endemic lizard of the Aeolian Islands(Mediterranean Sea). 223-229. In: Pérez-Mellado,V., Riera, N. & Perera, A. (eds.), The Biology ofLacertid Lizards. Evolutionary and EcologicalPerspectives. Institut Menorquí d’Estudis. Recerca,8. Mahón.

Bol. Asoc. Herpetol. Esp. (2006) 17 (1)

58

Martin, J.E. 2005. Helmintofauna de los lacértidosendémicos de las Islas Canarias: relacionesparásito-hospedador. Ph. D. Thesis University ofValencia.

Martin, J.E., Llorente, G.A., Roca, V., Carretero, M.A.,Montori, A., Santos, X. & Romeu, R. 2005.Relationships between diet and helminths in Gallotiacaesaris (Sauria: Lacertidae). Zoology, 108:121-130.

Pérez-Mellado, V. & Corti, C. 1993. Dietary adaptationsand herbivory in lacertid lizards of the genusPodarcis from western Mediterranean islands(Reptilia: Sauria). Bonner Zoologische Beiträge, 44:193-220.

Petter, A.J. & Quentin, J.C. 1976. Keys to generaOxyuroidea. 1-30. In: Anderson, R.C., Chabaud,A.G. & Willmot, S. (eds.), C.I.H. Keys to thenematode parasites of vertebrates. CommonwealthAgricultural Bureaux, Farnham Royal. Bucks.England.

Roca, V. 1985. Contribución al conocimiento de losparásitos de los lacértidos y gekónidos del pisotermomediterráneo del Levante ibérico. Ph. D.Thesis. University of Valencia.

Roca, V. 1993. Helmintofauna dels rèptils. 273-292. In:Alcover, J.A., Ballesteros, E. & Fornós, J.J. (eds.),Història Natural de l’arxipèlag de Cabrera.Monografies de la Societat d’Història Natural de lesBalears, 2. CSIC-Editorial Moll. Palma de Mallorca.

Roca, V. 1995. An approach to the knowledge of thehelminth infracommunities of Mediterranean insularlizards (Podarcis spp.). 285-292. In: Llorente, G.A.,Montori, A., Santos, X. & Carretero, M.A. (eds.),Scientia Herpetologica. AHE. Barcelona.

Roca, V. 1996. The effect of some factors on thehelminth parasite infracommunities of Podarcislizards in the Balearic Islands (WesternMediterranean). Bolletí de la Societat d’HistòriaNatural de les Balears, 39: 65-76.

Roca, V. 2004. Helminth component communities ofPodarcis pityusensis (Sauria: Lacertidae) fromisolated and non-isolated host populations. 293-298.In: Pérez-Mellado, V., Riera, N. & Perera, A. (eds.),The Biology of Lacertid Lizards. Evolutionary andEcological Perspectives. Institut Menorquí d’Estudis.Recerca, 8. Menorca.

Roca, V. & Hornero, M.J. 1994. Helminthinfracommunities of Podarcis pityusensis andPodarcis lilfordi (Sauria: Lacertidae) from theBalearic Islands (Western Mediterranean Basin).Canadian Journal of Zoology, 72: 658-664.

Schneider, B. 1997. Chalcides ocellatus (Forskal, 1775).312-313. In: Gasc, J.P. (ed.), Atlas of Amphibiansand Reptiles in Europe. SEH - Muséum Nationald’Histoire Naturelle. Paris.

Van Damme, R. 1999. Evolution of herbivory in lacertidlizards: effects of insularity and body size. Journal ofHerpetology, 33: 663-674.